Confirmation and Control of HPPD-Inhibiting Herbicide–Resistant Waterhemp (Amaranthus Tuberculatus) in Nebraska

Home , Acetochlor, Clopyralid, Dicamba, Dimethenamid, Glufosinate, Metolachlor

Weed Technology 2017 31:67–79 © Weed Science Society of America, 2017

Confirmation and Control of HPPD-Inhibiting Herbicide–Resistant Waterhemp (Amaranthus tuberculatus) in Nebraska

Maxwel C. Oliveira, Amit J. Jhala, Todd Gaines, Suat Irmak, Keenan Amundsen, Jon E. Scott, and Stevan Z. Knezevic*

Field and greenhouse experiments were conducted in Nebraska to (1) confirm the 4-hydroxyphenylpyruvate dioxygenase (HPPD)-inhibiting resistant-waterhemp biotype (HPPD-RW) by quantifying the resistance levels in dose-response studies, and (2) to evaluate efficacy of PRE-only, POST-only, and PRE followed by POST herbicide programs for control of HPPD-RW in corn. Greenhouse dose-response studies confirmed that the suspected waterhemp biotype in Nebraska has evolved resistance to HPPD-inhibiting herbicides with a 2- to 18-fold resistance depending upon the type of HPPD-inhibiting herbicide being sprayed. Under field conditions, at 56 d after ≥ treatment, 90% control of the HPPD-RW was achieved with− PRE-applied mesotrione/atrazine/ S-metolachlor + acetochlor, pyroxasulfone (180 and 270 g ai ha 1), pyroxasulfone/fluthiacet-methyl/ atrazine, and pyroxasulfone + saflufenacil + atrazine. Among POST-only herbicide programs, glyphosate, a premix of mesotrione/atrazine tank-mixed with diflufenzopyr/dicamba, or metribuzin, or glufosinate provided ≥92% HPPD-RW control. Herbicide combinations of different effective sites of action in mixtures provided ≥86% HPPD-RW control in PRE followed by POST herbicide programs. It is concluded that the suspected waterhemp biotype is resistant to HPPD-inhibiting herbicides and alternative herbicide programs are available for effective control in corn. The occurrence of HPPD-RW in Nebraska is significant because it limits the effectiveness of HPPD-inhibiting herbicides. Nomenclature: Acetochlor, atrazine, glyphosate, clopyralid, dicamba, diflufenzopyr, dimethenamid-P, flumetsulam, fluthiacet-methyl, glufosinate, isoxaflutole, mesotrione, metribuzin, pyroxasulfone S-metolachlor, saflufenacil, rimsulfuron, tembotrione, thiencarbazone-methyl, topramezone, waterhemp, Amaranthus tuberculatus (Moq.) Sauer, corn, Zea mays L. Key words: 4-hydroxyphenylpyruvate dioxygenase, pigment inhibitors, PRE, POST, triketone, weed management, weed resistance.

Se realizaron experimentos de campo y de invernadero en Nebraska para (1) confirmar un biotipo de Amaranthus tuberculatus resistente a inhibidores de 4-hydroxyphenylpyruvate dioxygenase (HPPD) (HPPD-RW) cuantificando el nivel de resistencia con estudios de respuesta a dosis, y (2) evaluar la eficacia de programas de herbicidas para el control de HPPD-RW en maíz con sólo herbicidas PRE, sólo POST, y herbicidas PRE seguidos por POST. Los estudios de respuesta a dosis en invernadero confirmaron que el biotipo de A. tuberculatus en Nebraska ha evolucionado resistencia a herbicidas inhibidores de HPPD con 2 a 18 veces mayor resistencia dependiendo del tipo de herbicida inhibidor de HPPD que se aplicó. Bajo condiciones de campo, a 56 d después del tratamiento, se alcanzó ≥90% de control de HPPD RW con aplicaciones PRE de mesotrione/ − atrazine/S-metolachlor + acetochlor, pyroxasulfone (180 y 270 g ai ha 1), pyroxasulfone/fluthiacet-methyl/atrazine, y pyroxasulfone + saflufenacil + atrazine. Entre los programas de herbicidas con sólo POST, glyphosate, una premezcla de mesotrione/ atrazine mezclados en tanque con diflufenzopyr/dicamba, o metribuzin, o glufosinate brindaron ≥ 92% control de HPPD-RW. Combinaciones de herbicidas efectivos con diferentes sitios de acción en mezclas brindaron ≥86% de control de HPPD-RW en programas de herbicidas PRE seguidos por POST. Se concluyó que el biotipo de A. tuberculatus es resistente a herbicidas inhibidores de HPPD y que hay programas de herbicidas alternativos disponibles para su control efectivo en maíz. La ocurrencia de HPPD-RW en Nebraska es significativa porque limita la efectividad de herbicidas inhibidores de HPPD.

DOI: 10.1017/wet.2016.4 *First, second, and ﬁfth authors: Graduate Student, Assistant Professor, and Assistant Professor, Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68583; Third author: Assistant Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO 80523; Fourth author: Professor, Department of Biological Systems Engineering, University of Nebraska, Lincoln, NE 68583; Sixth and seventh authors: Research Technologist and Professor, Northeast Research and Extension Center, Haskell Agricultural Laboratory, University of Nebraska–Lincoln, Concord, NE 68728. Corresponding author’s E-mail: [email protected]

Oliveira et al.: HPPD Resistant Waterhemp • 67

Downloaded from https:/www.cambridge.org/core. University of Nebraska Lincoln, on 15 Mar 2017 at 02:45:48, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/wet.2016.4 Waterhemp is a summer, annual, broadleaf species need for including the use of mixtures in herbicide native to the midwestern United States (Sauer 1967; programs to control HPPD-RW. The benefits of using Waselkov and Olsen 2014). Waterhemp has been herbicide mixtures are well documented, including identified as one of the most troublesome weeds over season-long weed control and a reduction in the risk of the past decade (Hager et al. 2002; Prince et al. 2012; herbicide resistance (Beckie and Reboud 2009; Butts Steckel and Sprague 2004). There are a variety of et al. 2016; Johnson et al. 2012; Kumar and Jha 2015; factors contributing to the rise of waterhemp as a Loux et al. 2011). problem weed, including adoption of no-tillage farming Failure of a POST-applied HPPD-inhibiting herbi- practices, extended germination period of waterhemp, cide to control waterhemp in a seed corn production decreased use of residual herbicides, and rapid spread operation was reported in eastern Nebraska in 2011. of multiple herbicide resistance (Culpepper 2006; Felix Therefore, we conducted a series of experiments to and Owen 1999; Hartzler et al. 1999). 1) confirm the presence of HPPD-RW and determine Waterhemp biotypes have evolved resistance to its level of resistance to POST-applied mesotrione, six herbicide site-of-action (SOA) groups, including tembotrione, and topramezone in dose-response acetolactate synthase inhibitors (Weed Science Society studies, and to 2) evaluate herbicide options for of America Site of Action [WSSA SAO] Group 2), control of HPPD-RW based on PRE-only, POST- synthetic auxins (WSSA SOA Group 4), triazines only, and PRE followed by (fb) POST herbicide (WSSA SOA Group 5), 5-enolpyruvylshikimate- programs. This information will be beneficial in the 3-phosphate synthase inhibitors (WSSA SOA Group development of alternative herbicide programs for 9), and protoporphyrinogen oxidase inhibitors (WSSA managing HPPD-RW in Nebraska. SOA Group 14) (Bernards et al. 2012; Heap 2016a; Sarangi et al. 2015; Tranel et al. 2011). In addition, just in the last six years it was confirmed that waterhemp Materials and Methods biotypes evolved resistance to4-hydroxyphenylpyruvate Plant Materials. In the fall of 2013, inflorescences dioxygenase (HPPD)-inhibiting herbicides (WSSA of waterhemp plants that survived repeated meso- SOA Group 27) in Illinois (Hausman et al. 2011) and trione and tembotrione applications were collected Iowa (McMullan and Green 2011). Therefore, new from a field near Columbus, Platte County, NE, herbicide options to manage waterhemp are needed and used as the suspected HPPD-RW. Waterhemp (Tranel et al. 2011). However, no new herbicide SOAs inflorescences collected in the fall of 2014 from a have been developed in recent years (Duke 2012). field in Clay County, NE with a history of effective The herbicides with the most recently developed control using the recommended rate of HPPD- SOA are the HPPD-inhibiting herbicides, intro- inhibiting herbicides were considered the HPPD- duced in the 1980s (Duke 2012; Mitchell et al. inhibiting herbicide–susceptible waterhemp biotype 2001). This herbicide group inhibits HPPD and (HPPD-SW), and used in this study for a compar- causes bleaching of green tissues of susceptible plants ison. Inflorescences of waterhemp were dried for (Grossmann and Ehrhardt 2007; Mitchell et al. 2 wk at room temperature (25 C). The seeds were 2001). Mesotrione, tembotrione, and topramezone cleaned and stored at 5 C until used in the green- are common POST-applied HPPD-inhibiting house study. Seeds were planted in 713-cm3 plastic herbicides, primarily used in corn (Bollman et al. pots containing a commercial potting mix (Berger 2008; Gitsopoulos et al. 2010; Nurse et al. 2010; BM1 All-Purpose Mix, Berger Peat Moss Ltd., Sutton et al. 2002). The recent occurrence of a Saint-Modest, Quebec, Canada). Emerged seedlings HPPD-inhibiting herbicide–resistant waterhemp (1 cm) were transplanted into 164-cm3 cone-tainers biotype (HPPD-RW) has increased the complexity (Ray Leach “Cone-tainer” SC10®, Stuewe and Sons of waterhemp control in corn (McMullan and Green Inc, Tangent, OR 97389) containing identical 2011). commercial potting mix described above. Plants were Control of a waterhemp biotype in Illinois that is supplied with adequate water and kept in greenhouse resistant to HPPD- and photosystem II–inhibiting conditions at 28/22 C day/night temperature. fi herbicides was not achieved using a single active Arti cial lighting was provided− − using metal halide ingredient of foliar or soil-applied herbicide (Hausman lamps (600 µmol photon m 2 s 1) to ensure a 16-h et al. 2015; Hausman et al. 2013); therefore, there is a photoperiod.

68 • Weed Technology 31, January–February 2017

Downloaded from https:/www.cambridge.org/core. University of Nebraska Lincoln, on 15 Mar 2017 at 02:45:48, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/wet.2016.4 Dose-Response Studies. Greenhouse dose-response B represents the biomass (g) of an individual treated bioassays were conducted in 2015 at the University of experimental unit. Nebraska–Lincoln to determine the resistance levels The effective dose needed to suppress the population of HPPD-RW and HPPD-SW sprayed with each of by 50% (ED50)and90%(ED90)forHPPD-RWand the three HPPD-inhibiting herbicides (mesotrione, HPPD-SW was determined using the three-parameter tembotrione, and topramezone). log-logisticcurveofthedrcpackageoftheRstatistical Each study had a completely randomized design with environment (Knezevic et al. 2007): four replications and was repeated twice. Separate Y = d = 1 + expfgb½logðÞx logðÞe : [2] experiments were conducted for the HPPD-RW and the HPPD-SW. The treatments were arranged in a In this model, Y is the control (%) or biomass reduction factorial treatment design with 3 herbicides and 6 rates. (%), d is the upper limit, and e represents the ED50 The herbicide rates for the HPPD-RW were 0, 0.5×, 1×, value. The parameter b is the relative slope around the −1 2×, 4×, and 8×, and for the HPPD-SW were 0, 0.25×, parameter e,andx is the herbicide dose in g ai ha . 0.5×, 0.75×, 1×, and 2×, where 1× represents either The resistance level was calculated by dividing the −1 105 g ai ha mesotrione (Syngenta Crop Protection, effective dose (ED50) of the HPPD-RW by the effective Research Triangle Park, NC 27709) plus 1% v/v of crop dose of the HPPD-SW. The resistance level indices for ® the respective effective dose between the HPPD-RW oil concentrate (Agri-Dex , Helena− Chemical Co., Collierville, TN 38017) and 20.5 g L 1 of ammonium and the HPPD-SW were compared using the EDcomp (or SI) function of package drc in R software (Ritz sulfate (DSM Chemicals− North America Inc., Augusta, GA 30901); 92 g ai ha 1 tembotrione (Bayer Crop and Streibig 2005). The EDcomp function compares Science, Research Triangle Park, NC 27709) plus 1% v/ the ratio of effective doses using t-statistics, where < v methylated seed oil (Noble®,Winfield Solutions, P-value 0.05 indicates that herbicide ED50 values are −1 different between the HPPD-RW and the HPPD-SW. Shoreview, MN 55126)− and 20.5 g L ammonium sulfate; or 24.5 g ai ha 1 topramezone (AMVAC, Los The Fligner-Killeen test of homogeneity was used to test the assumption of constant error variance among Angeles, CA− 90023) plus 1% v/v methylated seed oil and 20.5 g L 1 ammonium sulfate. data sets. This is a non-parametric test, which can Herbicide treatments were applied with a single- detect departures from normality in data (Conover tip chamber sprayer (DeVries Manufacturing et al. 1981). Corp, Hollandale, MN 56045) fitted with an 8001 E nozzle (Spraying Systems Co., North Efficacy of Herbicide Programs on HPPD- Avenue, Wheaton, IL 60139), calibrated to deliver RW. Field experiments were conducted in 2013 and −1 fi 140 L ha− spray volume at 210 kPa at a speed of 2014 at a Platte County eld location near Columbus, 3.7 km h 1. Waterhemp control was assessed visually NE (41.64°N, 97.58°W) where the HPPD-RW was 21 d after treatment (DAT) using a scale of 0% to reported. The soil type at the study location was a 100% (where 0 indicates no injury and 100 indicates siltyclayloam(12%sand,60%silt,28%clay)with plant death). Control ratings were based on symp- 3.3% organic matter and a pH of 6.8. Glyphosate- and ‘ toms such as bleaching, necrosis, and stunting of glufosinate-tolerant hybrid corn Golden− Harvest plants compared to non-treated plants. Aboveground H-9138’ was seeded at 79,280 seeds ha 1 in rows biomass was harvested at 21 DAT from each spaced 76 cm apart on May 16, 2013 and May 22, experimental unit and oven-dried at 65 C until 2014. Monthly mean air temperature and total reaching constant weight before weight of biomass precipitation data during the study periods are provided was recorded. The biomass (g) data were converted (Table 1). Experiments were conducted in a rando- into biomass reduction (%) compared with the mized complete block design with three replications non-treated experimental unit as: and 10, 6, and 16 treatments for PRE-only, POST-only, and PRE fb POST herbicide programs, % HPPD-RW biomass reduction respectively (Tables 2, 3, and 4). A 3 by 7.6 m plot was =½ðÞĒ B = Ē ´ 100; ½1 considered an experimental unit. Herbicide treatments were applied with a CO2- Ē where represents the mean biomass (g) of the pressurized− backpack sprayer calibrated to deliver non-treated experimental unit replicates, and 140 L ha 1 aqueous solution at 172 kPa (PRE) and

Oliveira et al.: HPPD Resistant Waterhemp • 69

Table 2. List of PRE-only herbicides used for control of HPPD-inhibiting herbicide-resistant waterhemp in field experiments conducted in 2013 and 2014 near Columbus, NE. Treatment Herbicidea Trade name Rate Manufacturer − gaiha1 1 Acetochlor/flumetsulam/clopyralid SureStart® 1,490 Dow Agrosciences, Indianpolis, IN 46268 2 Mesotrione/atrazine/ Lumaz EZ® 2,780 +1,470 Syngenta Crop Protection, Research S-metolachlor + acetochlor + Harness® Triangle Park, NC 27709 + Monsanto Company, St. Louis, MO 63167 3 Pyroxasulfone Zidua® 90 BASF Corporation, Research Triangle Park, NC 27709 4 Pyroxasulfone Zidua® 180 BASF Corporation 5 Pyroxasulfone Zidua® 270 BASF Corporation 6 Pyroxasulfone/fluthiacet-methyl/ Anthem 1,260 FMC Corporation, Philadelphia, PA atrazine ATZ® 19104. 7 Pyroxasulfone + saflufenacil Zidua® 149 + 75 + 560 BASF Corporation + atrazine + Sharpen® + BASF Corporation + AAtrex® + Syngenta Crop Protection 8Saflufenacil/dimethenamid- Verdict® 730 + 263 BASF Corporation P + dimethenamid-P + Outlook® + BASF Corporation 9 Thiencarbazone-methyl/isoxaflutole Corvus® 129 + 1,800 Bayer CropScience, Research Triangle Park, + atrazine + AAtrex® NC 27709 + Syngenta Crop Protection aAbbreviations: Herbicide premix (/); herbicide tankmix (+).

70 • Weed Technology 31, January–February 2017

Results and Discussion mesotrione are likely due to longer use history of mesotrione-based products for weed control at the Dose-Response Studies. Error variance among data research site. sets was constant. Treatment-by-experiment interac- McMullan and Green (2011) reported waterhemp tion was not significant; therefore data were combined. resistant to mesotrione in Iowa, but at a lower level of Dose-response studies confirmed that the resistance (8-fold). Differences in fold-level resistance waterhemp biotype was resistant to POST-applied between reported biotypes may partly be due to HPPD-inhibiting herbicides (mesotrione, tembotrione, variation in the sensitivity of the susceptible population and topramezone).− The labeled rate of mesotrione used in the study, and may also be due to the fact that (105 g ha 1) provided less than 40% control of the the waterhemp biotype from Iowa was also acetolactate HPPD-RW (Figure 1A). In addition, a mesotrione rate synthase– and triazine-resistant. In addition, HPPD −1 of 342 g ha was needed to achieve 50% (ED50) herbicide resistance level may be influenced by plant control of the HPPD-RW (Table 5), which is thirteen height at the time of application. The Iowa waterhemp times the rate required to control HPPD-SW. The biotype height at the time of application was 3 to 5 cm, ED90 was not calculated because 90% control was− not compared to 8 to 10 cm in this study. Furthermore, achieved even with the maximum rate (840 g ha 1)of multiple resistant populations of waterhemp in Illinois mesotrione tested in this study. A similar trend was also exhibited various resistance levels to mesotrione, evident with tembotrione (Figure 2A) and topramezone ranging 10- to 35-fold, depending upon the susceptible (Figure 3A), with the resistance level, based on ED50 population used for comparison (Hausman et al. 2011). values, estimated as 6-and 3-fold higher for HPPD-RW Palmer amaranth resistant to HPPD-inhibiting herbi- than for HPPD-SW, respectively. In contrast, the cides has also been confirmed in Nebraska (Jhala et al. HPPD-SW demonstrated sensitivity to all three 2014) and Kansas (Thompson et al. 2012). In HPPD-inhibiting herbicides applied POST: 90% Nebraska, it was reported that Palmer amaranth sprayed control (ED90) was achieved with the labeled rates when 10 cm tall was most resistant to topramezone (14- (Table 5). to 23-fold), followed by tembotrione (4- to 6-fold), and Dose-response curves based on biomass reduction mesotrione (4-fold) (Jhala et al. 2014). (%) suggest the same resistance level as do the data based on control (%) estimates (Figures. 1B, 2B, Efficacy of Herbicide Programs on HPPD- and 3B; Table 6). Based on biomass reduction (%), RW. Error variance among data sets was constant. the HPPD-SW was most resistant to mesotrione Treatment-by-year interaction was not significant for (18-fold), followed by tembotrione (5-fold), and the three field experiments; therefore, data were topramezone (2-fold). Higher resistance levels to combined.

Oliveira et al.: HPPD Resistant Waterhemp • 71

Table 4. List of PRE followed by POST herbicides used for control of HPPD-inhibiting herbicide-resistant waterhemp in ﬁeld experiments conducted in 2013 and • https:/www.cambridge.org/core 2014 near Columbus, Platte County, NE.

edTcnlg 1 January 31, Technology Weed Treatment Herbicidea Trade name Timing Rate Manufacturer Adjuvantb − g ai(ae) ha 1 1 Acetochlor/atrazine fb Harness Xtra® fb PRE fb 2,700 fb Monsanto Company fb glyphosate Roundup PowerMax® POST + 1,540 + 25 + 560 Monsanto Company MSO + AMS . https://doi.org/10.1017/wet.2016.4 + topramezone + atrazine + Impact® + AAtrex® + AMVAC, Commerce, CA 90040 + Syngenta Crop Protection 2 Acetochlor/atrazine fb Harness Xtra® fb PRE fb 2,700 fb Monsanto Company fb topramezone + diflufenzopyr/dicamba Impact® + Status® + AAtrex® POST 25 + 196 + 560 + AMVAC + BASF Corporation MSO + AMS . University of NebraskaLincoln + atrazine + Syngenta Crop Protection 3 Acetochlor/flumetsulam/clopyralid fb SureStart® fb PRE fb 1,490 fb Dow Agrosciences fb glyphosate Durango® POST 1,170 Dow Agrosciences AMS 4 Mesotrione/atrazine/S-metolachlor Lumaz EZ® + AAtrex® PRE fb 2,780 + 1,080 + 1,470 Syngenta Crop Protection + Syngenta + atrazine + acetochlor fb + Harness® fb fb Crop Protection + Monsanto Company fb diflufenzopyr/dicamba + atrazine Status® + AAtrex® POST 196 + 450 BASF Corporation + Syngenta Crop COC – Protection + AMS eray2017 February 5 Mesotrione/atrazine/S-metolachlor Lumaz EZ® + AAtrex® fb PRE fb 2,780 + 1,080 fb Syngenta Crop Protection + atrazine fb + Syngenta Crop Protection fb

, on diflufenzopyr/dicamba + glyphosate Status® + Touchdown Total® POST 196 + 1170 BASF Corporation AMS + Syngenta Crop Protection 15 Mar2017 at02:45:48 6 Mesotrione/atrazine/S-metolachlor Lumaz EZ® + AAtrex® fb PRE fb 2,780 + 1,080 fb Syngenta Crop Protection + atrazine fb + Syngenta Crop Protection fb glyphosate Touchdown Total® POST 1,170 Syngenta Crop Protection AMS 7 Mesotrione/atrazine/S-metolachlor Lumaz EZ® PRE fb 2,780 Syngenta Crop Protection + atrazine fb + AAtrex® fb + 1,080 fb + Syngenta Crop Protection fb atrazine + S-metolachlor + glufosinate AAtrex® + Dual II Magnum® POST 450 + 1,070 + 595 Syngenta Crop Protection AMS + Liberty 280® + Syngenta Crop Protection + Bayer Crop Science , subjectto theCambridgeCore termsofuse,available at 8 Mesotrione/atrazine/S-metolachlor fb Lumaz EZ® fb PRE fb 1,550 fb Syngenta Crop Protection fb atrazine + glyphosate/S-metolachlor/ AAtrex® + Halex® GT POST 1,080 + 2,220 Syngenta Crop Protection NIS + AMS mesotrione + Syngenta Crop Protection 9 Mesotrione/atrazine/S-metolachlor fb Lumaz EZ® fb PRE fb 2,780 fb Syngenta Crop Protection fb glyphosate Touchdown Total® POST 1,170 Syngenta Crop Protection AMS 10 Mesotrione/atrazine/S-metolachlor fb Lumaz EZ® fb PRE fb 2,780 fb Syngenta Crop Protection fb diflufenzopyr/dicamba Status® POST 98 BASF Corporation NIS 11 Mesotrione/atrazine/S-metolachlor fb Lumaz EZ® fb PRE fb 2,780 fb Syngenta Crop Protection fb diflufenzopyr/dicamba Status® POST 196 BASF Corporation NIS

12 Pyroxasulfone/fluthiacet-methyl/atrazine fb Anthem ATZ® fb PRE fb 1,260 fb FMC Corporation fb NIS pyroxasulfone/fluthiacet-methyl Anthem® POST 94 FMC Corporation 13 Rimsulfuron + S-metolachlor/atrazine fb Resolve DF® + Bicep II Magnum® PRE fb 18 + 3,240 DuPont, Wilmington, DE fb 19898 + Syngenta Crop Protection fb glyphosate Abundit Extra® POST 840 DuPont AMS 14 Saflufenacil/dimethenamid-P Verdict® + Outlook® fb PRE fb 730 + 263 fb BASF Corporation + dimethenamid-P fb + BASF Corporation fb topramezone + diflufenzopyr/dicamba Impact® + Status® POST 18 + 196 AMVAC + BASF Corporation NIS 15 Thiencarbazone-methyl/isoxaflutole + Corvus® + AAtrex® fb PRE fb 129 + 1,120 fb Bayer Crop Science + atrazine fb Syngenta Crop Protection fb diflufenzopyr/dicamba Status® POST 196 BASF Corporation NIS aAbbreviations: Herbicide premix (/); herbicide tankmix (+ ); fb, followed by. − b AMS, ammonium sulfate (20.5 g L 1; DSM Chemicals North America Inc., Augusta, GA 30901); COC, crop oil concentrate (1% v/v; Agridex®, Helena Chemical Co., Collierville, TN 38017); NIS, nonionic surfactant (0.25% v/v; Induce®, Helena Chemical Co., Collierville, TN 38017), MSO, methylated seed oil (1% v/v; Noble®, Winfield Solutions, Shoreview, MN 55126). Table 5. Estimated ED50 and ED90 values based on control (%) in 8- to 10-cm HPPD-inhibiting herbicide–resistant (HPPD-R) and susceptible (HPPD-S) waterhemp biotype at 21 d after treatment in a dose-response study with mesotrione, tembotrione, and topramezone conducted under greenhouse conditions at the University of Nebraska–Lincoln. HPPD-inhibiting herbicidesb

ED50 ED90 Resistance Biotypea (± SE) (± SE) P-valuec leveld − ______gaiha1 ______Mesotrione HPPD-SW 26 (2) 152 (17) - HPPD-RW 342 (28) - *** 13 Tembotrione HPPD-SW 11 (2) 57 (6) - HPPD-RW 61 (4) 673 (99) *** 6 Topramezone HPPD-SW 3 (0.5) 15 (2) - HPPD-RW 8 (1) 72 (10) *** 3 aAbbreviations: HPPD-SW, 4-hydroxyphenylpyruvate dioxygenase (HPPD)-inhibiting herbicide–susceptible waterhemp biotype collected from a ﬁeld in Clay County, NE in 2014; HPPD-RW, HPPD-inhibiting herbicide–resistant waterhemp biotype from a ﬁeld in Platte County, NE in 2013. b ED50, effective dose required to control 50% population; ED90, effective dose required to control 90% population. c Figure 1. Control of (A) and biomass reduction (B) of 8- to HPPD-RW vs HPPD-SW t-statistics comparison of ED50, α < 10-cm tall HPPD-inhibiting herbicide–resistant (HPPD-RW) *** 0.01. d and susceptible (HPPD-SW) waterhemp biotype at 21 d after Resistance level was calculated by dividing ED50 value of treatment with POST-applied mesotrione in dose-response stu- HPPD-RW by HPPD-SW for each herbicide. dies under greenhouse conditions.

PRE-Only Herbicide Program. PRE herbicides The HPPD-RW is neither acetolactate synthase evaluated in this study provided 51% to 96% control nor triazine resistant, and results of PRE-only

and density reduction of the HPPD-RW− (Table 7). herbicide programs suggest that PRE herbicide Pyroxasulfone applied alone at 270 g ha 1 and several options are available for effective control of the other PRE-applied herbicide mixtures with different HPPD-RW in corn. SOA (Treatments 1, 2, 6, 7, 8, and 9) provided ≥93% HPPD-RWcontrol at 30 and 41 DAT. At POST-Only Herbicide Program. Four POST ≥ 56 DAT, mesotrione/atrazine/− S-metolachlor, pyrox- herbicide programs provided 90% control of the asulfone (180 and 270 g h 1), and pyroxasulfone + HPPD-RW at 21 DAT with ≥84% density reduc- saﬂufenacil + atrazine provided 95% to 98% control tion at 35 DAT (Table 8). For example, glyphosate without difference among them. Moreover, at 56 (Treatment 1) provided ≥93% HPPD-RW control

DAT, there was no difference between− higher pyr- and density reduction. Thus, the HPPD-RW was oxasulfone rates (180 and 270 g ha 1) and pyrox- very sensitive to glyphosate due to the fact that asulfone applied in tank-mixtures with other the experimental site had been under seed corn herbicides (Treatments 6 and 7). Similarly, other production at least for last ﬁve years with no use studies have shown ≥90% control of pigweed species of glyphosate. Mesotrione/atrazine + diﬂufenzopyr/ with pyroxasulfone applied alone or in tank-mixtures dicamba (Treatment 2), mesotrione/atrazine + (Knezevic et al. 2009; Mahoney et al. 2014; Nurse glufosinate (Treatment 3), and mesotrione/atrazine + et al. 2010). metribuzin (Treatment 4) also provided 92% control

Oliveira et al.: HPPD Resistant Waterhemp • 73

Downloaded from https:/www.cambridge.org/core. University of Nebraska Lincoln, on 15 Mar 2017 at 02:45:48, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/wet.2016.4 Figure 2. Control of (A) and biomass reduction (B) of 8- to Figure 3. Control of (A) and biomass reduction (B) of 8- to 10-cm tall HPPD-inhibiting herbicide resistant (HPPD-RW) 10-cm tall HPPD-inhibiting herbicide resistant (HPPD-RW) and susceptible (HPPD-SW) waterhemp biotype at 21 d after and susceptible (HPPD-SW) waterhemp biotype at 21 d after treatment with POST-applied tembotrione in dose-response treatment with POST-applied topramezone in dose-response stu- studies under greenhouse conditions. dies under greenhouse conditions.

of HPPD-RW at 21 DAT. This is due to synergistic The results of POST-only herbicide programs effect of HPPD-inhibiting herbicides and photosystem indicated that glyphosate, and premix of mesotrione/ II–inhibiting herbicides (e.g., atrazine and metribuzin). atrazine tank mixed with synthetic auxins glufosinate Previous studies have conﬁrmed improved control of and metribuzin, are effective herbicide programs for Amaranthus species in corn by tank-mixing HPPD- control of HPPD-RW in corn. and photosystem II–inhibiting herbicides (Abendroth et al. 2006; Woodyard et al. 2009). PRE fb POST Herbicide Programs. Most PRE fb There was no difference in HPPD-RW control POST herbicide programs provided ≥ 83% control (21 DAT) between glyphosate and mesotrione/ and density reduction of HPPD-RW at 32 DAPOST atrazine in tank mixtures with diﬂufenzopyr/ (Table 9). The HPPD-RW was ≥86% controlled with dicamba, glufosinate, or metribuzin. All of these PRE herbicide 30 DAPRE. The HPPD-RW control ≥ −1 treatments resulted in 92% HPPD-RW control. (%) in PRE was higher when treated with 2,780− g ha Mesotrione/atrazine + metribuzin caused 15% tempor- (Treatments 9, 10, and 11) than 1,550 g ha 1 (Treat- ary stunting in corn at 10 DAT (data not shown). ment 8) of mesotrione/S-metolachlor/atrazine. Further- −1 Fluthiacet-methyl + mesotrione showed poor (53%) more, adding atrazine (1,080 g ha− ) to mesotrione/ control of the HPPD-RW at 21 DAT (Table 8). atrazine/S-metolachlor (2,780 g ha 1) did not improve

Similar results were obtained by Jhala et al. (2014), who the HPPD-RW control (%).− The mesotrione/atrazine/ reported that ﬂuthiacet-methyl used alone was not S-metolachlor (2,780 g ha 1) provided nearly complete effective in controlling Amaranthus species. or complete control of HPPD-RW. This mixture, with

74 • Weed Technology 31, January–February 2017

or without atrazine, resulted in ≥97% HPPD-RW and thiencarbazone-methyl/isoxaflutole + atrazine pro- control at 30 DAPRE. Moreover, acetochlor/flumetsu- vided ≥ 95% HPPD-RW control. lam/clopyralid, pyroxasulfone/fluthiacet-methyl/atra- Treatments fb POST application of glyphosate zine, saflufenacil/dimethenamid-P +dimethenamid-P, alone (Treatments 3, 6, 9, and 13) or glyphosate +

Table 7. Effect of PRE-only herbicide programs on HPPD-inhibiting resistant waterhemp control (%) and population density reduction (%) in field experiments conducted in 2013 and 2014 near Columbus, NE. b b HPPD-inhibiting herbicide-resistant Control Density reduction waterhempa DATa Treatment Herbicidec Rate 30 41 56 56 − gaiha 1 ______% ______1 Acetochlor/flumetsulam/clopyralid 1,490 93 bc 85 d 85 bc 91 bcd 2 Mesotrione/atrazine/S-metolachlor + acetochlor 2,780 + 1,470 97 a 98 a 96 a 98 a 3 Pyroxasulfone 90 83 d 63 e 51 d 70 e 4 Pyroxasulfone 180 90 cd 87 cd 91 ab 97 a 5 Pyroxasulfone 270 95 abc 94 abc 92 ab 95 abc 6 Pyroxasulfone/fluthiacet-methyl/atrazine 1,260 96 ab 94 abc 92 ab 88 cd 7 Pyroxasulfone + saflufenacil + atrazine 149 + 75 + 560 96 ab 97 ab 93 ab 96 ab 8Suflafenacil/dimethenamid-P + dimethenamid-P 730 + 263 96 ab 91 bcd 86 bc 84 d 9 Thiencarbazone-methyl/isoxaflutole + atrazine 129 + 1,800 90 cd 91 bcd 75 c 60 e P-valued *** *** *** *** aAbbreviations: DAT, d after treatment; HPPD, 4-hydroxyphenylpyruvate dioxygenase. The control (0%) data of non-treated experimental unit were not included in analysis. Density reduction (%) was calculated on the basis of comparison with density (plants m2) of non-treated experimental unit. bMeans presented within each column with no common letter(s) are significantly different according to Fisher’s Protected LSD test where P ≤ 0.05. cHerbicide premix (/); herbicide tankmix (+). dANOVA, ***α <0.01.

Oliveira et al.: HPPD Resistant Waterhemp • 75

topramezone + atrazine (Treatment 1), glyphosate + also help in fields with substantial waterhemp diflufenzopyr/dicamba (Treatment 5), and glypho- density, which has tendency to emerge over a longer sate/S-metolachlor/mesotrione + atrazine (Treatment period of time (Cordes et al. 2004; Schuster and 8) provided ≥ 95% HPPD-RW control and Smeda 2007). density reduction at 32 DAPOST. Diflufenzopyr/ This study confirmed the first case of HPPD-RW dicamba resulted in 86% to 91% control of in Nebraska, and the third in the United States HPPD-RW, but the control was improved to 97% (Heap 2016b). This biotype showed the highest when glyphosate was tank-mixed with diflufenzopyr/ resistance to mesotrione, followed by tembotrione dicamba (Treatment 5). Non-glyphosate treatments, and topramezone, most likely due to the longer including topramezone + diflufenzopyr/dicamba + history of mesotrione use at the study site in a atrazine (Treatment 2), diflufenzopyr/dicamba + atra- continuous seed corn production system. The results zine (Treatment 4), atrazine + S-metolachlor + glufosi- indicate that there are herbicide programs that nate (Treatment 7) and topramezone + diflufenzopyr/ have the potential to provide effective control of dicamba (Treatment 14) resulted in ≥94% HPPD- HPPD-RW in corn. Tactics for minimizing the risk RW control and density reduction at 32 DAPOST. of herbicide resistance should be based on the These results suggest that many herbicide options are principles of integrated weed management, especially available to manage HPPD-RW in corn, at least in utilizing mixtures or premixes of herbicides with Nebraska and the upper Midwest. different SOA. Despite availability of alternative Herbicide rotations and/or mixtures of active herbicides, the spread of HPPD-inhibiting herbicide ingredients that have different SOA have been resistance in Amaranthus spp. is increasing across recommended by researchers as a way to prevent other parts of Nebraska and the United States or delay the evolution of resistant weeds (Beckie (Hausman et al. 2011; Jhala et al. 2014; McMullan 2006; Gressel and Segel 1990; Norsworthy et al. and Green 2011; Thompson et al. 2012), which 2012; Wrubel and Gressel 1994). Similarly, Living- is of great concern because it limits the effectiveness ston et al. (2015) suggested that the lowest risk of of mesotrione, tembotrione, and topramezone on evolving herbicide resistance occurred when both pigweed species. Future research is needed to PRE and POST herbicide applications are part of a confirm the mechanism of resistance to HPPD- systematic approach to weed control. In addition, the inhibiting herbicides observed in this biotype from sequential application of PRE fb POST would Nebraska.

76 • Weed Technology 31, January–February 2017

Table 9. Effect of PRE followed by POST herbicide programs on HPPD-inhibiting herbicide–resistant-waterhemp control (%) and population density reduction (%) in https:/www.cambridge.org/core ﬁeld experiments conducted in 2013 and 2014 near Columbus, NE. Controlb Density reductionb HPPD-inhibiting herbicide–resistant waterhempa DAPREa DAPOSTa c

. Treatment Herbicide Timing Rate 30 32 32 https://doi.org/10.1017/wet.2016.4 − g ai (ae) ha 1 ______% ______1 Acetochlor/atrazine fb PRE fb 2,700 fb 96 abc 96 abc 97 ab . University of NebraskaLincoln Glyphosate + topramezone + atrazine POST 1,540 + 25 + 560 2 Acetochlor/atrazine fb PRE fb 2,700 fb 86 e 97 ab 98 a topramezone + diflufenzopyr/dicamba + atrazine POST 25 + 196 + 560 3 Acetochlor/flumetsulam/clopyralid fb PRE fb 1,490 fb 95 c 96 abc 97 ab Glyphosate POST 1,170 4 Mesotrione/atrazine/S-metolachlor + atrazine + acetochlor fb PRE fb 2,780 + 1,080 + 1,470 fb 98 a 97 ab 98 a diflufenzopyr/dicamba + atrazine POST 196 + 450 5 Mesotrione/atrazine/-S-metolachlor + atrazine fb PRE fb 2,780 + 1,080 fb 97 abc 97 ab 98 ab , on diflufenzopyr/dicamba + glyphosate POST 196 + 1,170 15 Mar2017 at02:45:48 6 Mesotrione/atrazine/S-metolachlor + atrazine fb PRE fb 2,780 + 1,080 fb 98 a 96 abc 98 a glyphosate POST 1,170 7 Mesotrione/atrazine/S-metolachlor + atrazine fb PRE fb 2,780 + 1,080 fb 97 abc 98 a 98 a atrazine + S-metolachlor + glufosinate POST 450 + 1,070 + 595 8 Mesotrione/atrazine/S-metolachlor fb PRE fb 1,550 fb 91 d 95 bdc 98 a atrazine + glyphosate/S-metolachlor/mesotrione POST 1,080 + 2,220 , subjectto theCambridgeCore termsofuse,available at

lviae l:HP eitn Waterhemp Resistant HPPD al.: et Oliveira 9 Mesotrione/atrazine/S-metolachlor fb PRE fb 2,780 fb 98 a 97 ab 97 ab glyphosate POST 1,170 10 Mesotrione/atrazine/S-metolachlor fb PRE fb 2,780 fb 97 abc 91 de 95 bc diflufenzopyr/dicamba POST 98 11 Mesotrione/atrazine/S-metolachlor fb PRE fb 2,780 fb 97 abc 96 abc 97 ab diflufenzopyr/dicamba POST 196 12 Pyroxasulfone/fluthiacet-methyl/atrazine fb PRE fb 1,260 fb 96 abc 87 e 92 c pyroxasulfone/ fluthiacet-methyl POST 94 13 Rimsulfuron + S-metolachlor/atrazine fb PRE fb 18 + 3,240 fb 88 de 97 ab 97 ab glyphosate POST 840 14 Saflufenacil/dimethenamid-P + dimethenamid-P PRE fb 730 + 263 fb 96 abc 94 cd 97 ab topramezone + diflufenzopyr/dicamba POST 18 + 196 15 Thiencarbazone-methyl/isoxaflutole + atrazine fb PRE fb 129 + 1,120 fb 96 abc 86 e 83 d diflufenzopyr/dicamba POST 196 P-valued *** *** *** aAbbreviations: DAPRE, d after PRE; DAPOST, d after POST; HPPD, 4-hydroxyphenylpyruvate dioxygenase. The control (%) data of non-treated experimental unit − were not included in analyses. Density reduction (%) was calculated on the basis of comparison with density (plants m 2 ) of non-treated experimental unit. bMeans presented within each column with no common letter(s) are significantly different according to Fisher’s Protected LSD test where P ≤ 0.05. c

• Herbicide premix (/); herbicide tankmix (+ ); fb, followed by. d α <

77 ANOVA, *** 0.01. Acknowledgments Hausman NE, Singh S, Tranel PJ, Riechers DE, Kaundun SS, Polge ND, Thomas DA, Hager AG (2011) Resistance to The authors thank CAPES (Brazilian Government ‐ o HPPD inhibiting herbicides in a population of waterhemp Foundation) - Proc. n 9112-13-8, for financial (Amaranthus tuberculatus) from Illinois, United States. Pest support to the graduate student involved in this Manag Sci 67:258–261 study. We appreciate the help of Sergio Oliveira, Hausman N, Tranel P, Riechers D, Hager AG (2015) Responses Kyle Kardell, and Amanda Winstead in this project. of a waterhemp (Amaranthus tuberculatus) population resistant to HPPD-inhibiting herbicides to foliar-applied herbicides. 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